Evidence of a divided nutritive function in the rainbow trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach

Authors: BETIKU, OMOLOLA - Florida A & M University; YEOMAN, CARL - Montana State University; GAYLORD, T. GIBSON - Us Fish And Wildlife Service; ISHAQ, SUZANNE - Montana State University; DUFF, G - New Mexico State University; Sealey, Wendy

Submitted to: Aquaculture Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/17/2023
Publication Date: 6/1/2023
Citation: Betiku, O., Yeoman, C., Gaylord, T., Ishaq, S., Duff, G., Sealey, W.M. 2023. Evidence of a divided nutritive function in the rainbow trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach. Aquaculture Reports. 30. Article 101601. https://doi.org/10.1016/j.aqrep.2023.101601.
DOI: https://doi.org/10.1016/j.aqrep.2023.101601

Interpretive Summary: To improve our understanding of the rainbow trout gastrointestinal tract (GIT) microbiome, ARS researchers at the Bozeman Fish Technology Center collaborated with Montana State University faculty and students to perform shotgun metagenomic analyses on the luminal contents from both mid- and hind-GIT regions of fish fed two dietary treatments (non-aquatic animal- or a plant based-protein source). The results of this study support a nutritive role for trout GIT microbes and indicate a potential division of nutritive functions between the mid- and hind-GIT microbiomes, and in some respects, adaptable to the fish diet. This is a novel report on applying the whole shotgun metagenomic approach to analyzing the gut microbiome of rainbow trout, a cornerstone aquaculture species. Most available reports on trout gut microbiome used 16S rRNA-based approaches. The report highlights and identifies the potential nutritive contributions of GIT microbes to trout and a potentially crucial functional division along the GIT. These differences appear to be partially modulated by differences in diet compositions and, in some respects, adaptable to the fish diet. The study revealed that trout respond well to diets with alternative animal and plant protein sources when supplemented with essential amino acids to meet the requirements of the fish.

Technical Abstract: The nutritive role and ecology of gut-dwelling microbes in rainbow trout remain enigmatic. To improve our understanding of the rainbow trout gastrointestinal tract (GIT) microbiome, we performed whole shotgun metagenomic analyses on the luminal contents from both mid- and hind-GIT regions of fish fed two dietary treatments (non-aquatic animal- or a plant based-protein source). A total of 1,278,287,800 raw reads were assembled. Microbes were predominantly bacteria (89.9%) and mainly of the phyla Tenericutes, Firmicutes, Fusobacteria, and Proteobacteria. Eukaryotic (8.8%) microbes were mainly from phyla Ascomycota and Basidiomycota, while Archaea (<1%) were also present and predominantly from the phylum Euryarchaeota. Comparisons of genus-level classifications and functional profiles revealed compositional differences in these GIT locations that appear modulated by differences in the dietary treatments. The functional analysis provided evidence of amino acid biosynthesis/catabolism and methane production in the mid-GIT, while in the hind-GIT, proteolytic hydrolysis and butyrate metabolism were expressed in the trout fed with plant protein. The animal protein-based diet provided metabolites for microbial protein fermentation in the hind-GIT. The results of this study support a nutritive role for trout GIT microbes and indicate a potential division of nutritive functions between the mid- and hind-GIT microbiomes, and in some respects, adaptable to the fish diet.